Evaluation of PGPR strains on wheat yield and quality parameters

<strong>Evaluation</strong> <strong>of</strong> <strong>PGPR</strong> <strong>strains</strong> on wheat yield and quality
parameters
Metin Turan 1 , Medine Güllüce 2 , Güleray AĞAR 2 Fikrettin Sahin 3*
1 Ataturk University, Faculty <strong>of</strong> Agriculture, Department <strong>of</strong> Soil Science and Plant Nutrition,
Erzurum 25240, Turkey
2 Ataturk University, Faculty <strong>of</strong> Science, Department <strong>of</strong> Biology, Erzurum 25240, Turkey
3* Yeditepe University, Faculty <strong>of</strong> Engineering and Architecture, Department <strong>of</strong> Genetics and
Bioengineering, Kayisdagi, Istanbul 34755, Turkey
Corresponding author: m_turan25@hotmail.com
Abstract
N 2 -fixing and P-solubilizing bacteria are important in plant nutrition increasing N and P uptake
by the plants, and playing a significant role as plant growth-promoting rhizobacteria (<strong>PGPR</strong>)
in the bi<strong>of</strong>ertilization <strong>of</strong> crops. In 2007 and 2008, a field study was conducted in two different
locations (Erzurum and Ispir) in the Eastern part <strong>of</strong> Turkey for investigating the effects <strong>of</strong> two
N 2 -fixing and P-solubilizing <strong>PGPR</strong> <strong>strains</strong> alone and in combinations on plant yield and
nutrient content <strong>of</strong> wheat (Triticum aestivum L.) in comparison to control and optimum and
half doses <strong>of</strong> N fertilizer application under field condition. All inoculations and fertilizer
applications significantly increased grain yield (GY), straw yield (SY), total yield (TY), and
macro and micro nutrients <strong>of</strong> wheat over the control. Mixed <strong>PGPR</strong> inoculations with the strain
<strong>of</strong> OSU-142 + M3 + Azospirillum Sp245 has significantly increased grain yield <strong>of</strong> wheat as
good as full doses <strong>of</strong> nitrogen. The highest leaf, grain, and straw N and S contents were
obtained from mixed inoculation (with the OSU-142 + M3 + Azospirillum Sp245 ) +40 kg N
ha -1 , but P, K, Mn, Fe, and Zn contents were obtained from Bacillus M3 treatment. The data
suggested that seed inoculation with OSU-142 + M3 + Azospirillum Sp245 may reduce
fertilizer rates down to 50% in wheat production.
Key words: Inoculation; grain yield, plant growth-promoting rhizobacteria; macro and micro
element
1. Introduction
Nitrogen and phosphorus are known to be essential nutrients for plant growth and
development. Intensive farming practices that achieve high yield require chemical fertilizers,
which are not only costly but may also create environmental problems. A group <strong>of</strong> bi<strong>of</strong>ertilizers
called plant growth promoting rhizobacteria (<strong>PGPR</strong>) (Kloepper et al. 1980) contain
<strong>strains</strong> from genera such as Pseudomonas, Azospirillium, Azotobacter, Bacillus,
Burkholderia, Enterobacter, Rhizobium, Erwinia and Flavobacterium (Rodriguez and Fraga
1999). Thus organisms are important for agriculture in order to promote the circulation <strong>of</strong>
plant nutrients and reduce the need from chemical fertilizers. Most <strong>of</strong> the studies reporting
beneficial effects <strong>of</strong> the above mentioned <strong>PGPR</strong> were carried out in warm and subtropical
climates with favorable ambient temperatures. These bacteria may not be effective in cold
temperature conditions. Therefore, a study was conducted in order to investigate the effects
<strong>of</strong> alone and in combinations with N 2 -fixing and P-solubilizing <strong>PGPR</strong> <strong>strains</strong> on nodulation,
plant growth, nutrient uptake and grain yield <strong>of</strong> wheat in the cold highland (Erzurum) and low
land ( Ispir) plateaus.
2. Material and methods
The experiments were conducted using a randomized complete block design in a
factorial arrangement each having 10 main treatments as control (without inoculation
1

and any fertilizer application), Nitrogen (80 kg N ha -1 ), Nitrogen (40 kg N ha -1 ),
Bacillus OSU-142, Bacillus M3, Azospirillum sp. 245, Mixed (OSU-142 + M3+
Azospirillum Sp245), Bacillus megaterium RC07, Paenibacillus polymyxa RC05 and
Raoultella terrigena for 2007 and 7 treatment also added in 2008, Burkholderia
cepacia OSU7, OSU142 AMP Res, M3 Amp Res, Sp245 Amp Res, P. polymyxa 2/2,
B. megaterium T17, and Mixed + 40 kg N ha -1 . Wheat (Triticum aestivum spp.
vulgare var. Kirik) was sown in 7 m x 4 m plots having 34 rows so as to give 18 kg
seeds da -1 (430 seeds per m 2 ) on 10 and 17 May in 2007, 4 and 2 May in 2008 at site
I and site II. Maximum care has been taken not to contaminate and mix bacterial
inoculations during sowing. The data were subjected to analysis <strong>of</strong> variance (ANOVA)
using SPSS 13.0 (SPSS Inc., 2004) statistical program. Since “year x treatment”
interaction was not significant in many parameters evaluated, data were combined
over years, and means were presented. Mean values were separated according to
LSD test at P=0.05.
3. Result
3.1.Yield and yield parameters
The results showed that GY, SY, harvest index (HI) and TY <strong>of</strong> wheat cultivars in each
<strong>of</strong> two locations in both years significantly increased by N 2 -fixing and P-solubilizing <strong>PGPR</strong>
<strong>strains</strong> application compared with the control. The lowest GY, SY, TY and HI were recorded
in the control treatment and the bacterial inoculations increased GY by 8.6-43.7%, SY by
1.82.-12.9%, TY by 1.93- 19.80% and HI by 1.33-45.7% over the control on 2-year average
at two locations, respectively (Table 1). The GY <strong>of</strong> plant in 2007 was higher than GY <strong>of</strong> 2008,
but the highest TY <strong>of</strong> wheat was found in 2008 at each location (Table 1). The highest GY
(3.68-2.88 Mg ha -1 ), SY (9.73-8.57 Mg ha -1 ), and TY (13.41-11.45 Mg ha -1 ) in both years
average at two locations were obtained from 80 kg N ha -1 , and followed by in combination
(OSU-142 + M3+ Azospirillum Sp245) treatment at 3.47-2.87 Mg ha -1 for GY, 8.73-6.75 Mg
ha -1 for straw and 12.20-9.65 Mg ha -1 for total yields, respectively (Table 1). In other words,
mixed <strong>PGPR</strong> inoculations with the strain <strong>of</strong> OSU-142 + M3 + Azospirillum Sp245 has
significantly increased GY, SY, TY and HI <strong>of</strong> wheat as good as full doses <strong>of</strong> nitrogen. When it
is compared to 40 kg N ha -1 treatment, bio-fertilizer applicants were more effective to
increase the grain yield. On the other hand harvest index (HI) <strong>of</strong> two years average in two
locations was better in inoculation treatments in comparison to the control and mineral
fertilizer (80 and 40 kg N ha -1 ) treatments. While the lowest HI values were recorded in the
control treatment, the highest value was obtained from the OSU-142 + M3+ Azospirillum
Sp.245 and Bacillus M3 treatments. The yield and plant growth enhancement effects <strong>of</strong>
bacteria used in this study on wheat could be explained with N 2 -fixing and P-solubilizing
capacity <strong>of</strong> bacteria. The positive effects <strong>of</strong> the OSU-142 and M3 on the yield and growth <strong>of</strong>
crops such as sweet cherry, spinach, tomatoes, sugar beet, barley and wheat were
explained by N 2 -fixation ability, phosphate solubilizing capacity, indole acetic acid (IAA) and
antimicrobial substance production (Esitken et al., 2002; 2003; 2006; Turan et al., 2005;
Sahin et al., 2004; Elkoca et al., 2008). In the present study, it was also found that the
inoculation <strong>of</strong> <strong>PGPR</strong> <strong>strains</strong> increased N, P, K, S, Fe, Mn, and Zn content <strong>of</strong> wheat, which
provide the additional evidence supporting the finding <strong>of</strong> previous study. Two years <strong>of</strong> trials
under the field conditions indicated that mixed inoculation with OSU-142 + M3 + Azospirillum
Sp245 increased wheat GY, SY, TY and HI by two years average at 31.7%, 7.5%, and 13.4
% over the control, respectively. N 2 -fixing and P-solubilizing <strong>PGPR</strong> <strong>strains</strong> alone had also
significant effect on seed yield and yield component but were lower value than mixed
inoculation When compared to mineral fertilizer treatments, mixed inoculations has
significantly increased GY <strong>of</strong> wheat as good as full doses <strong>of</strong> nitrogen. Similar result was
obtained previous studies that combined culture inoculants significantly increased grain yield
as compared with single inoculation <strong>of</strong> individual organisms (Elkoca et al., 2008).
3.2.Effects <strong>of</strong> bio-fertilizer on plant nutrient element (PNE) contents <strong>of</strong> different parts
<strong>of</strong> the plant
2

N 2 -fixing and P-solubilizing <strong>PGPR</strong> <strong>strains</strong> application promoted PNE contents <strong>of</strong> different
parts <strong>of</strong> the plant. Although the highest leaf, grain, and straw N contents were obtained from
mixed inoculation with the OSU-142 + M3 + Azospirillum Sp245 +40 kg N ha -1 , which
increased N contents <strong>of</strong> leaf, grain and straw <strong>of</strong> plant by 52.6%, 83.4%, and 83.0% ,
respectively, compared with the control treatment. While S contents were obtained from
treatment OSU-142 + M3 + Azospirillum Sp245 and increasing rate were 64.9% for grain and
65.0% for straw. P, K, Mn, Fe, and Zn contents were obtained from Bacillus M3 treatment,
and increase rate for leaf, grain and straw <strong>of</strong> plant were 42.7%, 50.6%, 82.5% for P, 26.3%,
112.0%, 110.0% for K, 49.1%, 121.2%, 120.0% for Mn, 90.1%, 102.6%, 105.2% for Fe, and
49.2%, 75.4%, 75.4% for Zn (Table 2, grain and straw nutrient data was not given). The
concentrations <strong>of</strong> plant nutrients measured were generally within the accepted critical levels
(Jones et al. 1991; Mills and Jones,1996). PNE contents was varied in different parts <strong>of</strong> the
plant, as compared the nutrient concentration in part <strong>of</strong> the plant, these sequences for N, S,
Mn, Zn, Cu and Fe found most <strong>of</strong>ten were leaf> grain> straw, for P, and Mg were grain>leaf>
straw, and for K, and Ca straw> leaf> grain.
Enhancement <strong>of</strong> mineral uptake by plants should result in an increased accumulation
<strong>of</strong> both dry matter and minerals in the stem and leaves <strong>of</strong> the plant. During the reproductive
period, the accumulated minerals would be transferred to the reproductive parts <strong>of</strong> the plants
(Bashan et al., 1990). The present study, for the first time, demonstrates increased P, K and
micro-nutrient such as Mn, Fe, and Zn concentrations in field-grown wheat grain, straw and
leaf as a result <strong>of</strong> Bacillus megaterium (M3) inoculations. Some <strong>of</strong> the previous studies with
the same <strong>PGPR</strong> <strong>strains</strong> tested on chickpea, barley, raspberry, apricot and sweet cherry have
been reported similar findings confirming our data in the present work. The use <strong>of</strong> the OSU-
142 and M3 in chickpea (Elkoca et al., 2008), raspberry (Orhan et al., 2006), apricot (Esitken
et al., 2003), sweet cherry (Esitken et al., 2006) and strawberry (Güneş et al, 2009)
stimulated macro- and micro-nutrient uptake such as N, P, K, Ca, Mg, Fe, Mn, Zn, Cu.
The higher N content in the treatments containing OSU-142 + M3 + Azospirillum
Sp245 +40 kg N ha -1 and OSU-142 may have resulted from the N 2 -fixation ability <strong>of</strong> these
bacterium, as reported in the other studies (Cakmakci et al., 2007; Elkoca et al., 2008). It is
well known that increasing N content in plants results in greater uptake <strong>of</strong> nutrient elements
from soil (Marschner, 1995). This evidence confirms the data showing that the percentage <strong>of</strong>
macro- and micro-nutrients was significantly and/or relatively increased in the bacteriatreated
plants, which may be explained by higher concentration <strong>of</strong> N 2 stimulated by bacterial
application. Orhan et al. (2006) reported that bacterial inoculations with OSU-142 and M3
decreased pH level <strong>of</strong> experimental soil from 6.7 to 5.6-6.0. decreased soil pH stimulates the
availability <strong>of</strong> PNE such as P, Ca, Fe and Mn. Additionally, it has also been reported that
OSU-142 and M3 increased root length and weight in some crops such as barley (Cakmakci
et al., 2007) and chickpea (Elkoca et al., 2008). It is also well known that efficient utilization
<strong>of</strong> PNE by a crop depends, to a large extent, on the amount <strong>of</strong> roots that contact the nutrient,
as well as the capacity <strong>of</strong> the root to absorb the contacted nutrient (Adepetu and Akapa,
1977).
4.Conclusions
Our results indicated that microbial inoculation <strong>of</strong> seeds with N 2 -fixing and P-solubilizing
<strong>PGPR</strong> <strong>strains</strong> alone and in combination, may substitute costly NP fertilizer in wheat
production even in cold highland and low land areas. In view <strong>of</strong> environmental pollution in
case <strong>of</strong> excessive use <strong>of</strong> fertilizers and due to high costs in the production <strong>of</strong> N and P
fertilizers, bacteria tested in our study may well be suited alone or in combination to achieve
sustainable and ecological agricultural production in the region. An important nutritional
problem <strong>of</strong> developing countries is micro-nutrient malnutrition, also called hidden hunger. Our
results also indicated that alone or in combination inoculations with N 2 -fixing and P-
solubilizing <strong>PGPR</strong> <strong>strains</strong> could increase mineral concentration and accumulations in the
grain. This paper supports the view that inoculations with <strong>PGPR</strong> have some potential to
serve as a means to reduce hidden hunger trough enhanced mineral concentration and
accumulation in grain.
3

Acknowledgements
We are very grateful to EU FP6-FOOD-CT-2006, STREP Project: RHIBAC for their generous
financial support for this study.
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Table 1 Yield and yield components <strong>of</strong> wheat plant growth <strong>of</strong> two locations in 2008 and 2007 (t ha -1 )
Inoculants I. Field II. Field
Grain Straw Total biomass Grain Straw Total biomass
Control (without inoculation and fertilizer) 2.79 c 7.79d 10.58 c 1.20 g 7.11b 8.31abc
(3.34 d)* (6.57 e) (9.90 d) (2.46 d) (8.90 c) (11.35 c)
Nitrogen (80 kg N ha -1 ) 4.18 a** 8.90 a 13.08a 1.95 a 8.51a 10.46 a
(4.02 a) (8.82 a) (12.83a) (3.34 a) (10.66 a) (14.00 a)
Nitrogen ( 40 kg N ha -1 ) 3.57 a-c 7.46d 11.03bc 1.58 cd 8.25a 9.83 ab
(3.79 a-c) (7.87 b) (11.66 ab) (2.27 ab) (11.07 a) (13.33 ab)
Bacillus OSU-142 3.35 a-c 8.37 a-c 11.72 a-c 1.53 cde 6.18bc 7.72 bcd
(3.69 a-d) (7.47 bc) (11.15 bc) (3.02 a-c) (9.04 b) (12.06 bc)
Bacillus M3 3.65 a-c 7.03d 10.68 c 1.50 cde 5.51 d 7.01 cd
(3.50 b-d) (6.69 e) (10.18 d) (2.85 c) (7.98 d) (10.83 c)
Azospirillum Sp245 4.17 a 7.78d 11.95 a-c 1.39 ef 4.70 e 6.09 d
(3.76 a-c) (8.07a) (11.83 a) (3.04 a-c) (9.18 b) (12.22 bc)
OSU-142 + M3 + Azospirillum Sp245 3.94 ab 8.68 ab 12.62ab 1.80 b 4.83 e 6.63 cd
(3.85 ab) (8.04a) (11.89 a) (3.10 a-c) (9.41 b) (12.51a-c)
Bacillus megaterium RC07 3.28 a-c 8.41 bc 11.69a-c 1.66 bc 6.65 bc 8.31 abcd
(3.43 cd) (7.39 cd) (10.83 c) (2.87 c) (8.26 c) (11.13 c)
Paenibacillus polymyxa RC05 3.81a-c 8.02 bc 11.83a-c 1.39 ef 6.39 bc 7.77 bcd
(3.72 a-c) (7.52 bc) (11.24 bc) (2.93 bc) (8.69 c) (11.61 bc)
Raoultella terrigena 3.59 a-c 7.37d 10.96bc 1.39 ef 5.71 d 7.09 cd
Burkholderia cepacia OSU7 2.99 bc 7.47d 10.46 c 1.59 c 7.35b 8.94 abc
OSU142 AMP Res 3.67 a-c 8.23 a-c 11.90a-c 1.49 cde 6.27bc 7.77 bcd
M3 Amp Res 3.54 a-c 8.19 a-c 11.73 a-c 1.53 cde 6.53 bc 8.06bcd
Sp245 Amp Res 3.20 a-c 8.52 a-c 11.72 a-c 1.42 def 8.49a 9.90 ab
P. polymyxa 2/2 3.20 a-c 8.92ab 12.12 a-c 1.39 ef 6.25bc 7.64 bcd
B. megaterium T17 3.41 a-c 8.42 a-c 11.83 a-c 1.30 fg 6.63bc 7.93 bcd
6

OSU-142 + M3 + Azospirillum sp245 +40 kg N ha -1 3.83 a-c 8.92a 12.75a 1.66 bc 4.47 e 6.12 d
* Data for 2007, **Averages <strong>of</strong> same column values (each section separately) followed by same letter did not differ significantly from Duncan’s
multiple range test at 0.5% significant
Table 2. Average leaf macro and micro element contents <strong>of</strong> wheat plant growth at two locations
Inoculants N Ca Mg Na K S Fe Mn Zn Cu P
% mg kg -1
Control 2.74 d* 3555 de 1262 h 631 a 5925 def 2061 de 33.5 f 62.7 d 38.4 e 19.9 e 3041f
80 kg N ha -1 3.68 abc 4675 b 1337 h 431 f 6807 b 2711 b 43.0 e 84.7 b 51.9 c 26.9 b 3673 cd
40 kg N ha -1 3.40 bcd 2915 gh 1662 fg 432 f 6051 cde 1690 gh 34.7 f 93.5 a 62.7 a 29.7 a 3906 bc
OSU-142 3.78 ab 2695 hı 1612 fg 581 b 6448 bc 1563 hı 41.7 e 75.9 c 46.5 d 24.1 c 2409 hı
M3 3.27 bcd 5795 a 1862 cd 280 h 7483 a 3361 a 63.7 b 93.5 a 57.3 b 29.8 a 4340 a
Sp245 3.30 bcd 3135 fg 1712 efg 556 c 5169 gh 1818 fg 55.8 c 67.1 d 41.1 e 21.3 de 3357 e
OSU-142 + M3
+Sp245
3.15 bcd 4235 c 1962 bc 431 f 5673 ef 2456 c 51.2 cd 75.9 c 46.6 d 24.2 c 3989 b
RC07 3.21 bcd 5775 a 2312 a 581 b 6177 cd 3349 a 55.0 c 89.1 ab 62.8 a 28.3 ab 3357 e
RC05 3.27 bcd 4455 bc 2012 b 431 f 6429 bc 2583 bc 54.2 c 75.9 c 46.5 d 24.1 c 3673 cd
R. terrigena 2.99 bcd 3355 ef 1762 def 531 cd 4917 h 1945 ef 47.2 de 93.5 a 57.3 b 29.7 a 3989 b
OSU7 3.31 bcd 3135 fg 1712 efg 381 g 6303 cd 1818 fg 46.2 de 67.1 d 41.2 e 21.3 de 3515 de
OSU142 AMP Res 3.05 bcd 2915 gh 1662 fg 431 f 5673 fe 1690 gh 62.3 b 75.9 c 46.6 d 24.1 c 2725 g
M3 Amp Res 2.89 cd 3795 d 1862 cd 506 de 6429 bc 2201 d 73.5 a 89.1 ab 54.7 bc 28.3 ab 3896 bc
Sp245 Amp Res 3.24 bcd 4675 b 2062 b 581 b 5673 ef 2711 b 45.3 e 93.5 a 62.7 a 29.7 a 2725 g
P. polymyxa 2/2 3.08 bcd 3575 de 1812 de 431 f 5547 fg 2073 de 41.8 e 75.9 c 46.6 d 24.1 c 2567 gh
B. megaterium T17 3.24 bcd 2475 ı 1562 g 381 g 6177 cd 1435 ı 44.5 e 67.1 d 41.1 e 21.3 de 3357 e
OSU-142 + M3+
Sp245 +40 kg N ha -1 4.18 a 3176 fg 1628 g 379 g 5219 gh 1842 fg 42.1 e 64.5 d 41.1 e 22.7 cd 2194 ı
*Averages <strong>of</strong> same column values (each section separately) followed by same letter did not differ significantly from Duncan’s multiple range test
at 0.5% significant
7